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Agricultural over-fertilization may adversely impact plant−microbial interactions affecting crop yield. It is unclear if soil microbiomes respond quickly to changes in fertilizer inputs once conditioned to specific nutrient regimes. We conducted a growth chamber study assessing the compositional and functional resilience of root-associated microbiomes of Medicago sativa to nutrient regime changes, and consequences for plant growth. Plants were grown with a common starting soil microbiome under four nutrient treatments: control (no fertilizer), organic phosphorus (compost added), low inorganic P (low triple superphosphate, TSP) and high inorganic P (high TSP). After several conditioning generations, in which microbiomes from rhizospheres of high biomass plants were transferred forward, microbiome composition was distinct across the four treatments. The resulting microbiomes were then transplanted into each of the nutrient treatments, leading generally to functional changes in hydrolytic enzyme activity and taxonomic convergence with other microbiomes transplanted into the same nutrient regime. However, high inorganic P-conditioned microbiomes were resistant to compositional change. Correspondingly, M. sativa grown with high inorganic P-conditioned microbiomes had lower biomass, fewer nodules, and lower %N than plants grown under the same nutrient regime with other microbiomes. These findings suggest that excessive inorganic P fertilization may change microbiomes such that they negatively affect plant growth.

Summary Climate change‐related soil salinization increases plant stress and decreases productivity. Soil microorganisms are thought to reduce salt stress through multiple mechanisms, so diverse assemblages could improve plant growth under such conditions. Previous studies have shown that microbiome selection can promote desired plant phenotypes, but with high variability. We hypothesized that microbiome selection would be more consistent in saline soils by increasing potential benefits to the plants. In both salt‐amended and untreated soils, we transferred forward Brassica rapa root microbiomes (from high‐biomass or randomly selected pots) across six planting generations while assessing bacterial (16S rRNA) and fungal (ITS) composition in detail. Uniquely, we included an add‐back control (re‐adding initial frozen soil microbiome) as a within‐generation reference for microbiome and plant phenotype selection. We observed inconsistent effects of microbiome selection on plant biomass across generations, but microbial composition consistently diverged from the add‐back control. Although salt amendment strongly impacted microbial composition, it did not increase the predictability of microbiome effects on plant phenotype, but it did increase the rate at which microbiome selection plateaued. These data highlight a disconnect in the trajectories of microbiomes and plant phenotypes during microbiome selection, emphasizing the role of standard controls to explain microbiome selection outcomes.

Summary Understanding the processes guiding microbial community assembly in soils is essential for predicting microbiome structure and function following soil disturbance events like agricultural soil fumigation. However, assembly outcomes are complex and variable, being affected by both selective abiotic forces and by the history of colonizing microorganisms. To untangle the interactions between these factors, we conducted a controlled microcosm study tracking bacterial assembly in cleared soils over 7 weeks. We used mesh bags to connect five unsterilized source soils, differing in land use history (forested, agricultural, or fallow), with four sterile recipient soil treatments, differing in abiotic conditions (no soil additives, salt addition, urea addition, or mixed salt/urea addition). We found that 59%–96% of bacterial colonizers after 1 week were Firmicutes, but by 7 weeks Actinobacteria and Bacteroidetes were also dominant. Salt and nitrogen additions reshaped bacterial assembly by constraining alpha diversity by up to half and biomass accumulation by up to an order of magnitude. Within‐treatment dispersion was significantly lower for salt and nutrient addition microcosms, suggesting deterministic selective pressures. In contrast, source soil origin had little impact on assembly trajectories. These results suggest that abiotic conditions can overshadow microbial source history in shaping community assembly outcomes.

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Microbial movement is important for replenishing lost soil microbial biodiversity and driving plant root colonization, particularly in managed agricultural soils, where microbial diversity and composition can be disrupted. Despite abundant survey-type microbiome data in soils, which are obscured by legacy DNA and microbial dormancy, we do not know how active microbial pools are shaped by local soil properties, agricultural management, and at differing spatial scales. To determine how active microbial colonizers are shaped by spatial scale and environmental conditions, we deployed microbial traps (i.e. sterile soil enclosed by small pore membranes) containing two distinct soil types (forest; agricultural), in three neighboring locations, assessing colonization through 16S rRNA gene and fungal ITS amplicon sequencing. Location had a greater impact on fungal colonizers (R2 = 0.31 vs. 0.26), while the soil type within the microbial traps influenced bacterial colonizers more (R2 = 0.09 vs. 0.02). Bacterial colonizers showed greater colonization consistency (within-group similarity) among replicate communities. Relative to bacterial colonizers, fungal colonizers shared a greater compositional overlap to sequences from the surrounding local bulk soil (R2 = 0.08 vs. 0.29), suggesting that these groups respond to distinct environmental constraints and that their in-field management may differ. Understanding how environmental constraints and spatial scales impact microbial recolonization dynamics and community assembly are essential for identifying how soil management can be used to shape agricultural microbiomes.